Superglue from bacteria: Unbreakable bridges for protein nanotechnology

Trends in Biotechnology

Volumn 32, Issue 10, 2014, Pages 506-512

  Veggiani, Gianluca ^a   Zakeri, Bijan ^b   Howarth, Mark ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Biomimetic; Mechanobiology; Nanobiotechnology; Protein engineering; Supramolecular assembly; Synthetic biology

Indexed keywords

BACTERIA; BIOLOGICAL MATERIALS; BIOMIMETICS; LIVING POLYMERIZATION; NANOBIOTECHNOLOGY; NANOTECHNOLOGY;

ADHESION PROTEINS; MECHANO-BIOLOGY; PEPTIDE-PROTEIN INTERACTIONS; PROTEIN ENGINEERING; STREPTOCOCCUS PYOGENES; SUPRAMOLECULAR ASSEMBLIES; SYNTHETIC BIOLOGY; WEAK INTERACTIONS;

PEPTIDES;

AMIDE; BIOMATERIAL; PEPTIDE; PROTEIN; ADHESIN; RECOMBINANT PROTEIN;

BACTERIUM; CANCER CELL; COVALENT BOND; NANOTECHNOLOGY; NONHUMAN; POLYMERIZATION; PROTEIN ASSEMBLY; PROTEIN INTERACTION; REVIEW; STREPTOCOCCUS PYOGENES; BIOTECHNOLOGY; CHEMICAL STRUCTURE; PROTEIN ENGINEERING;

ADHESINS, BACTERIAL; BIOTECHNOLOGY; MODELS, MOLECULAR; NANOTECHNOLOGY; PROTEIN ENGINEERING; RECOMBINANT PROTEINS; STREPTOCOCCUS PYOGENES;

EID: 84908025236     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2014.08.001     Document Type: Review

References (56)

1. Sletten E.M., Bertozzi C.R. Bioorthogonal chemistry: fishing for selectivity in a sea of functionality. Angew. Chem. 2009, 48:6974-6998.
2. Rashidian M., et al. Enzymatic labeling of proteins: techniques and approaches. Bioconjug. Chem. 2013, 24:1277-1294.
3. Huh W.K., et al. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
4. London N., et al. The structural basis of peptide-protein binding strategies. Structure 2010, 18:188-199.
5. Wood D.W. New trends and affinity tag designs for recombinant protein purification. Curr. Opin. Struct. Biol. 2014, 26C:54-61.
6. Huang J., et al. Structural basis for exquisite specificity of affinity clamps, synthetic binding proteins generated through directed domain-interface evolution. J. Mol. Biol. 2009, 392:1221-1231.
7. Lu Y., et al. Affinity-guided covalent conjugation reactions based on PDZ-peptide and SH3-peptide interactions. Bioconjug. Chem. 2014, 25:989-999.
8. Swift J.L., et al. A two-photon excitation fluorescence cross-correlation assay for a model ligand-receptor binding system using quantum dots. Biophys. J. 2006, 90:1396-1410.
9. Chivers C.E., et al. A streptavidin variant with slower biotin dissociation and increased mechanostability. Nat. Methods 2010, 7:391-393.
10. Fletcher J.M., et al. Self-assembling cages from coiled-coil peptide modules. Science 2013, 340:595-599.
11. Kent S.B. Total chemical synthesis of proteins. Chem. Soc. Rev. 2009, 38:338-351.
12. Shah N.H., Muir T.W. Inteins: nature's gift to protein chemists. Chem. Sci. 2014, 5:446-461.
13. Carvajal-Vallejos P., et al. Unprecedented rates and efficiencies revealed for new natural split inteins from metagenomic sources. J. Biol. Chem. 2012, 287:28686-28696.
14. Rossi E.A., et al. Complex and defined biostructures with the dock-and-lock method. Trends Pharmacol. Sci. 2012, 33:474-481.
15. Mao H., et al. Sortase-mediated protein ligation: a new method for protein engineering. J. Am. Chem. Soc. 2004, 126:2670-2671.
16. Strijbis K., et al. Protein ligation in living cells using sortase. Traffic 2012, 13:780-789.
17. Husnjak K., Dikic I. Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu. Rev. Biochem. 2012, 81:291-322.
18. Klock C., Khosla C. Regulation of the activities of the mammalian transglutaminase family of enzymes. Protein Sci. 2012, 21:1781-1791.
19. Dhillon E.K.S., et al. Host range, immunity and antigenic properties of lambdoid coliphage-Hk97. J. Gen. Virol. 1980, 50:217-220.
20. Wikoff W.R., et al. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 2000, 289:2129-2133.
21. Kang H.J., et al. Stabilizing isopeptide bonds revealed in Gram-positive bacterial pilus structure. Science 2007, 318:1625-1628.
22. Kang H.J., Baker E.N. Intramolecular isopeptide bonds: protein crosslinks built for stress?. Trends Biochem. Sci. 2011, 36:229-237.
23. Dutton R.J., et al. Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:11933-11938.
24. Stamnaes J., et al. The propensity for deamidation and transamidation of peptides by transglutaminase 2 is dependent on substrate affinity and reaction conditions. Biochim. Biophys. Acta 2008, 1784:1804-1811.
25. Zavalova L.L., et al. Destabilase from the medicinal leech is a representative of a novel family of lysozymes. Biochim. Biophys. Acta 2000, 1478:69-77.
26. Hagan R.M., et al. NMR spectroscopic and theoretical analysis of a spontaneously formed Lys-Asp isopeptide bond. Angew. Chem. 2010, 49:8421-8425.
27. Hu X., et al. Autocatalytic intramolecular isopeptide bond formation in Gram-positive bacterial pili: a QM/MM simulation. J. Am. Chem. Soc. 2011, 133:478-485.
28. Charville H., et al. The uncatalyzed direct amide formation reaction - mechanism studies and the key role of carboxylic acid H-bonding. Eur. J. Org. Chem. 2011, 5981-5990.
29. Shekhawat S.S., Ghosh I. Split-protein systems: beyond binary protein-protein interactions. Curr. Opin. Chem. Biol. 2011, 15:789-797.
30. Zakeri B., Howarth M. Spontaneous intermolecular amide bond formation between side chains for irreversible peptide targeting. J. Am. Chem. Soc. 2010, 132:4526-4527.
31. Oke M., et al. The Scottish Structural Proteomics Facility: targets, methods and outputs. J. Struct. Funct. Genomics 2010, 11:167-180.
32. Amelung S., et al. The FbaB-type fibronectin-binding protein of Streptococcus pyogenes promotes specific invasion into endothelial cells. Cell. Microbiol. 2011, 13:1200-1211.
33. Zakeri B., et al. Peptide tag forming a rapid covalent bond to a protein, through engineering a bacterial adhesin. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E690-E697.
34. Li L., et al. Structural analysis and optimization of the covalent association between SpyCatcher and a peptide tag. J. Mol. Biol. 2014, 426:309-317.
35. Fierer J.O., et al. SpyLigase peptide-peptide ligation polymerizes affibodies to enhance magnetic cancer cell capture. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:E1176-E1181.
36. Zhang W.B., et al. Controlling macromolecular topology with genetically encoded SpyTag-SpyCatcher chemistry. J. Am. Chem. Soc. 2013, 135:13988-13997.
37. Matsunaga R., et al. Hyperthin nanochains composed of self-polymerizing protein shackles. Nat. Commun. 2013, 4:2211.
38. Abe H., et al. Split Spy0128 as a potent scaffold for protein cross-linking and immobilization. Bioconjug. Chem. 2013, 24:242-250.
39. Rago F., Cheeseman I.M. Review series: the functions and consequences of force at kinetochores. J. Cell Biol. 2013, 200:557-565.
40. Zhang X., et al. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science 2009, 324:1330-1334.
41. Stroka K.M., Konstantopoulos K. Physical biology in cancer. 4. Physical cues guide tumor cell adhesion and migration. Am. J. Physiol. 2014, 306:C98-C109.
42. Alegre-Cebollada J., et al. Isopeptide bonds block the mechanical extension of pili in pathogenic Streptococcus pyogenes. J. Biol. Chem. 2010, 285:11235-11242.
43. Moore S.W., et al. Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev. Cell 2010, 19:194-206.
44. Wong J., et al. Direct force measurements of the streptavidin-biotin interaction. Biomol. Eng. 1999, 16:45-55.
45. Popa I., et al. Nanomechanics of HaloTag tethers. J. Am. Chem. Soc. 2013, 135:12762-12771.
46. Kufer S.K., et al. Covalent immobilization of recombinant fusion proteins with hAGT for single molecule force spectroscopy. Eur. Biophys. J. 2005, 35:72-78.
47. Beyer M.K., Clausen-Schaumann H. Mechanochemistry: the mechanical activation of covalent bonds. Chem. Rev. 2005, 105:2921-2948.
48. Bornschlogl T., Rief M. Single-molecule protein unfolding and refolding using atomic force microscopy. Methods Mol. Biol. 2011, 783:233-250.
49. Chen A.Y., et al. Synthesis and patterning of tunable multiscale materials with engineered cells. Nat. Mater. 2014, 13:515-523.
50. Liu D.S., et al. Quantum dot targeting with lipoic acid ligase and HaloTag for single-molecule imaging on living cells. ACS Nano 2012, 6:11080-11087.
51. Howarth M., et al. Monovalent, reduced-size quantum dots for single molecule imaging of receptors in living cells. Nat. Methods 2008, 5:397-399.
52. Yu M., et al. Circulating tumor cells: approaches to isolation and characterization. J. Cell Biol. 2011, 192:373-382.
53. Jain J., et al. Cholesterol loading and ultrastable protein interactions determine the level of tumor marker required for optimal isolation of cancer cells. Cancer Res. 2013, 73:2310-2321.
54. Iwai H., Pluckthun A. Circular beta-lactamase: stability enhancement by cyclizing the backbone. FEBS Lett. 1999, 459:166-172.
55. Schoene C., et al. SpyTag/SpyCatcher cyclization confers resilience to boiling on a mesophilic enzyme. Angew. Chem. Int. Ed. Engl. 2014, 53:6101-6104.
56. Hyre D.E., et al. Cooperative hydrogen bond interactions in the streptavidin-biotin system. Protein Sci. 2006, 15:459-467.